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Brock/Springer Series in Contemporary Bioscience
Comparative Ecology of Microorganisms
and Macroorganisms
Brock/Springer Series in Contemporary Bioscience
Series Editor: Thomas D. Brock University of Wisconsin-Madison
Tom Fenchel ECOLOGY OF PROTOZOA: The Biology of Free-living Phagotrophic Protists
Johanna Diibereiner and Fabio O. Pedrosa NITROGEN-FIXING BACTERIA IN NONLEGUMINOUS CROP PLANTS
Tsutomu Hattori THE VIABLE COUNT: Quantitative and Environmental Aspects
Roman Saliwanchik PROTECTING BIOTECHNOLOGY INVENTIONS: A Guide for Scientists
Hans G. Schlegel and Botho Bowien (Editors) AUTOTROPHIC BACTERIA
Barbara Javor HYPERSALINE ENVIRONMENTS: Microbiology and Biogeochemistry
Ulrich Sommer (Editor) PLANKTON ECOLOGY: Succession in Plankton Communities
Stephen R. Rayburn THE FOUNDATIONS OF LABORATORY SAFETY: A Guide for the Biomedical Laboratory
Gordon A. McFeters (Editor) DRINKING WATER MICROBIOLOGY: Progress and Recent Developments
Mary Helen Briscoe A RESEARCHER'S GUIDE TO SCIENTIFIC AND MEDICAL ILLUSTRATIONS
Max M. Tilzer and Colette Serruya (Editors) LARGE LAKES: Ecological Structure and Function
Jiirgen Overbeck and Ryszard J. Chr6st (Editors) AQUATIC MICROBIAL ECOLOGY: Biochemical and Molecular Approaches
John H. Andrews COMP ARA TIVE ECOLOGY OF MICROORGANISMS AND MACRO ORGANISMS
John H. Andrews
Comparative Ecology of Microorganisms
and Macroorganisms With 59 Figures and 14 Tables
Springer-Verlag
New York Berlin Heidelberg London Paris Tokyo Hong Kong Barcelona
John H. Andrews Department of Plant Pathology University of Wisconsin Madison, Wisconsin 53706, USA
Cover illustration: Kandis Elliot
Library of Congress Cataloging-in-Publication Data Andrews, John H. Comparative ecology of microorganisms and macroorganisms / by John H. Andrews
p. em - (Brock/Springer series in contemporary bioscience) Includes bibliographical references and index. ISBN-13: 987-1-4612-7786-6 e-ISBN-13: 987-1-4612-3074-8 001: 10.1007/987-1-4612-3074-8 1. Microbial ecology. 2. Ecology. I. Title. II. Series.
QR100.A53 1991 576'.15-dc20 90-19686
Printed on acid-free paper.
© 1991 Springer-Verlag New York Inc. Softcover reprint of the hardition 1st edition 1991
All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer-Verlag New York, Inc., 175 Fifth Avenue, New York, NY 10010, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use of general descriptive names, trade names, trademarks, etc., in this publication, even if the former are not especially identified, is not to be taken as a sign that such names, as understood by the Trade Marks and Merchandise Marks Act, may accordingly be used freely by anyone.
Production and editorial supervision: Science Tech Publishers.
987654321
ISBN-13: 987-1-4612-7786-6
In memory of my mother and father and for I.A.S.
Writing a book is an adventure: To begin with it is a toy, then amusement, then it becomes a mistress, then it becomes a master, and then it becomes a tyrant, and the last phase is that just as you are about to become reconciled to your servitude, you kill the monster and strew him about to the public.
-WINSTON CHURCHILL
Preface The most important feature of the modern synthetic theory of evolution is its foundation upon a great variety of biological disciplines.
-G.L. STEBBINS, 1968, p. 17
This book is written with the goal of presenting ecologically significant analogies between the biology of microorganisms and macroorganisms. I consider such parallels to be important for two reasons. First, they serve to emphasize that however diverse life may be, there are common themes at the ecological level (not to mention other levels). Second, research done with either microbes or macroorganisms has implications which transcend a particular field of study. Although both points may appear obvious, the fact remains that attempts to forge a conceptual synthesiS are astonishingly meager. While unifying concepts may not necessarily be strictly correct, they enable one to draw analogies across disciplines. New starting points are discovered as a consequence, and new ways of looking at things emerge.
The macroscopic organisms ('macroorganisms') include most representatives of the plant and animal kingdoms. I interpret the term 'microorganism' (microbe) literally to mean the small or microscopic forms of life, and I include in this category the bacteria, the protists (excluding the macroscopic green, brown, and red algae), and the fungi. Certain higher organisms, such as many of the nematodes, fall logically within this realm, but are not discussed at any length. Most of the microbial examples are drawn from the bacteria and fungi because I am most familiar with those groups, but the concepts they illustrate are not restrictive.
Because the intended audience includes individuals who are interested in 'big' organisms and those interested in 'small' organisms, I have tried to provide sufficient background information so that specific examples used to
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illustrate the principles are intelligible to both groups without being elementary or unduly repetitious to either. Evolutionary biologists in either camp may also find the work of interest because the central premise is that organisms have been shaped by evolution operating through differential reproductive success. Survivors would be expected to show some analogies in 'tactics' developed through natural selection. The only background assumed is a comprehensive course in college biology. Hence, the book is also appropriate for advanced undergraduates.
The need for a synthesis of plant, animal, and microbial ecology is apparent from an historical overview (e.g., McIntosh 1985). Plant ecology was originally almost exclusively descriptive. It remains so to a large degree. A strongly predictive science has emerged, but one based largely on correlation rather than causation (Harper 1984). Within the past few decades it has branched into three main streams: phytosociology, population biology, and the physiological or biophysical study of individual plants (Cody 1986).
In contrast, animal ecologists have tended to study groups of ecologically similar species (i.e., guilds; Cody 1986). Although animal ecologists have probably been the most influential in developing the field of population ecology, many of their mathematical models derive from work based on microorganisms (e.g., Gause 1932), and from medical epidemiology (again involving microorganisms). Zoologists have also been the main force behind ecological theory, particularly as it applies to communities. Significantly, in both plant and animal ecology, the processes underlying patterns are usually inferred: The evidence marshalled is typically correlative rather than causative, and frequently the difference between the two is overlooked, if recognized.
Many microbial ecologists study systems. Ecology as practiced by microbiologists, however, has been mainly autecology, is typically reductionist in the extreme (increasingly often at the level of the gene), and lacks the strong theoretical basis of macroecology. Microbiology is a diverse field and microbial ecologists may be protozoologists, bacteriologists, mycologists, parasitologists, plant or animal pathologists, epidemiologists, phycologists, or molecular biologists. Approaches and semantics differ considerably among these subdisciplines. Nevertheless, microbial ecology is in general like plant ecology in its strong descriptive element. For example, often the goal is to identify and quantify the members of a particular community. Despite increasing emphasis on field research in the last few decades, microbes are usually brought into and remain within the laboratory for study under highly controlled conditions to determine the genetic, biochemical, growth rate, or sporulation characteristics, or the pathological attributes of a particular population, and how these are influenced by various factors. Thus, the major operational difference between microorganisms and macroorganisms is that the former must generally be cultured to understand their properties. It is this requirement that brings the microbial ecologist so quickly from the field to the laboratory.
Preface ix
To oversimplify, one could say that macroecology consists of phenomena in search of mechanistic explanation, whereas microbial ecology is experimentation in search of theory.
The foregoing picture is reinforced by observations on the parochialism evident in science. Examples include the streamlined makeup of most professional societies, the narrow disciplinary affiliation of participants at a typical conference, or the content of many journals and textbooks. Microbes as illustrations of ecological phenomena are omitted from the mainstream of ecology texts and are mentioned in cursory fashion only insofar as they relate to nutrient cycling or to macroorganisms. Discussion is left for microbiologists to develop in books on 'microbial ecology', which in itself suggests that there must be something unique about being microscopic. This is not meant as criticism, but rather as an observation on the state of affairs and an illustration of the gulf between disciplines. Finally, if additional evidence were necessary, one need only reflect on the current furor about the release of genetically engineered organisms. To a large degree this contentious issue has polarized along disciplinary lines: Ecologists express concern that microbiologists have little real knowledge of 'ecology'; microbiologists respond that ecologists really do not understand microbial systems. While acknowledging obvious differences between the two groups of organisms, one must ask whether their biology is so distinct that such isolationism is warranted. This book addresses that question.
A synthesis of microbial ecology and macroecology could be attempted at the level of the individual, the population, or the community. There would be gains and losses with any choice. Even the use of all three hierarchical levels would not ensure absence of misleading statements. Relative to the individual, comparisons based on populations or communities offer considerably increased scope and allow for inclusion of additional properties emerging at each level of complexity (e.g., density of organisms at the population level or diversity indices at the community level). Parallels based, for example, on supposed influential (Le., organizing) forces in representative communities would be precarious, however, because unambiguous data implicating the relative roles of particular forces such as competition are usually lacking. The data that do exist have been variously interpreted, often with intense debate. Moreover, the same type of community may be organized quite differently in various parts of the world. For example, barnacle communities in Scotland (Connell 1961) are structured differently from those in the intertidal zone of the California coastline (Roughgarden et al. 1988). Entirely different pictures could emerge depending on the communities of microbes and macroorganisms arbitrarily selected for comparison.
Thus, I have decided to focus comparisons at the level of the individual. This implies neither that the individual is the only level on which selection acts, nor that shortcomings of the sort noted above do not exist. However, I consider the individual (defined in Chapter 1) through its entire life cycle to
x Preface
be operationally the fundamental unit of ecology in the sense that it is the primary one on which natural selection acts. Strictly speaking, natural selection acts at many levels, and a proper analysis of this issue requires that a distinction be made between what is transmitted and what transmits (Gliddon and Gouyon 1989). Efforts to relate the former (genetic information, broadly construed to include genes and epigenetic information) to a particular organizational level in a biological hierarchy extending from a nucleotide sequence to an ecosystem have engendered lively debate (e.g., Chapter 6 in Bell 1982; Brandon 1984; Tuomi and Vuorisalo 1989a,b; Gliddon and Gouyon 1989; Dawkins 1989). Without extending this controversy here, I note that at least my choice of the individual as the relevant ecological unit in this context is consistent with the conventional ecological viewpoint expressed by naturalists from Darwin onward (e.g., Dobzhansky 1956; Williams 1966; Mayr 1970, 1982; Begon et al. 1986; Ricklefs 1990). Comparisons of traits at the level of the individual can then be carried either downward to the corresponding genes-which have passed the screen of natural selection-or upward to assess the role of selection of traits at the group level.
This book proceeds first, by developing a common format (in Chapter 1) for comparing organisms; second, by contrasting (in subsequent chapters) the biology of macro- and microorganisms within that context; third (and also in the subsequent chapters), by drawing ecologically useful analogies, that is, parallels of interpretive value in comparisons of·traits or 'strategies' between representative organisms. The first two phases can be accomplished relatively objectively; the third is necessarily subjective. There are situations where macroorganisms provide the wrong model for microbes or vice versa. I have tried to avoid forcing the parallels and have stated where close parallels simply do not exist.
All citations appear in a bibliography at the end of the work. Where books are cited in the text, I also specify, when appropriate, the specific chapters or pages concerned, in order to assist the reader in locating the relevant passages. Finally, at the conclusion of each chapter, a few suggestions are made for additional reading on each particular topic.
This is a book mainly of ideas. I find that the study of analogs is instructive and productive, not to mention interesting and frequently exciting. There is considerable speculation and a strong emphasis on generalizations, which I hope will prove stimulating and useful to the reader. Inevitably, there will be exceptions to any of the general statements. I am not particularly concerned by these oddities and think that it would be a mistake for the book to be read with the intent of finding the exception in each case in an effort to demolish the principle. However, this is not the same as advocating that it be read uncritically! MacArthur and Wilson (1967, p.5) have said that even a crude theory, which may account for about 85% of the variation in a phenomenon, is laudable if it points to relationships otherwise hidden, thus stimulating new forms of research. Williams (1966, p.273) points out that every
Preface xi
one of Dalton's six postulates about the nature of atoms eventually turned out to be wrong, but because of the questioning and experimentation that resulted from them, they stand as a beacon in the advance of chemistry. Finally and most explicitly, Bonner (1965, p.15) states,
It is, after all, quite accepted that in a quantitative experiment, a statistical significance is sufficient to show a correlation. The fact that there are a few points that are off the curve, even though the majority are on it, does not impel one to disregard the whole experiment. Yet when we make generalizations about trends among animals and plants, such as changes in size, it is almost automatic to point out the exceptions and throw out the baby with the bath [sic]. This is not a question of fuzzy logic or sloppy thought; it is merely a question whether [sic] the rule or the deviations from the rule are of significance in the particular discussion.
I started this book during a sabbatical leave in 1986-1987 with John L. Harper, to whom I am deeply indebted for his generosity and kindness. His enthusiasm, innumerable ideas, and critical insight have contributed much to what is presented here. I thank R. Whitbread and the faculty of the School of Plant Biology at the University College of North Wales in Bangor, Wales, U.K. for putting up with me for a year; in particular I acknowledge with appreciation the hospitality of N.R. and C. Sackville Hamilton, the help of Michelle Jones in many ways, and the wise counsel of Adrian Bell. Finally, I thank the many colleagues elsewhere who have helped in various ways: G. Bowen, J. Burdon, D. Ingram, and J. Parke read a draft prospectus for the book. Aspects I have discussed with P. Ahlquist, J. Handelsman, and D. Shaw. I am grateful to the following individuals who have commented on one or more of the chapters: C. Allen, A. Bell, G. Carroll, K. Clay, A. Dobson, 1. Eastwood, A. Ellingboe, R. Evert, J. Farrow, r. Forge, J. Gaunt, J. Harper, M. Havey, R. Jeanne, D. Jennings, L. Kinkel, W. Pfender, G. Roberts, N. Sackville Hamilton, B. Schmid, and K. Willis. Errors of fact or interpretation remain mine.
I thank my editor, r.D. Brock, for constructive criticism and for encouraging me to write this book. I am indebted to Kandis Elliot for the outstanding artwork, Ruth Siegel for copyediting, Steve Heinemann for assistance with the computer graphics, and Steve Vicen for some of the photographs. Finally, I thank my family for their forbearance.
J.H.A. Bangor, Wales and Madison, Wisconsin
Contents
Preface vii
1 Introduction: Prospects for a Conceptual Synthesis 1 1.1 Differences and Similarities 1 1.2 A Framework for Comparison 5 1.3 What is an Individual? 12 1.4 Summary 16 1.5 Suggested Additional Reading 17
2 Genetic Variation 19 2.1 Introduction 19 2.2 Mechanisms 20 2.3 Sex and Meiotic Recombination 35 2.4 Somatic Variation and the Concept of the Genet 53 2.5 Summary 60 2.6 Suggested Additional Reading 62
3 Nutritional Mode 65 3.1 Introduction 65 3.2 What is a Resource? 65
xiii
xiv Contents
3.3 Some Fundamental Resource Categories and Their Implications 66
3.4 Resource Acquisition 76 3.5 Summary 97 3.6 Suggested Additional Reading 99
4 Size 101 4.1 Introduction 101 4.2 Constraints on Natural Selection: Phylogenetic,
Ontogenetic, and Allometric 103 4.3 Why Are There Macroorganisms? 104 4.4 On Seeing the World As an Elephant or a
Mycoplasma 113 4.5 Some Correlates of Size 119 4.6 Some Ecological Consequences of Size 126 4.7 Size and Life History Theory 133 4.8 Summary 141 4.9 Suggested Additional Reading 143
5 Growth and Growth Form 145 5.1 Introduction 145 5.2 Unitary and Modular Organisms: An Overview 146 5.3 Fungi As Modular Organisms 149 5.4 Bacteria As Modular Organisms 151 5.5 Some Implications of Being Modular 152 5.6 Some Implications to Modular Organisms of Being
Sessile 158 5.7 Form in the Natural World 169 5.8 Summary 175 5.9 Suggested Additional Reading 177
6 The Life Cycle 179 6.1 Introduction 179 6.2 Simple Versus Complex Life Cycles 179 6.3 Senescence 190 6.4 Summary 206 6.5 Suggested Additional Reading 207
7 The Environment 209 7.1 Introduction 209 7.2 The Environment and Organism Are Coupled 210
Contents xv
7.3 How Organisms Experience Environments 210 7.4 How Organisms Respond to Environments 215 7.5 Traffic Lights Regulate Progress Through the Life
Cycle 224 7.6 Habitable Sites and the Evolution of Gene Flow 227 7.7 Summary 234 7.8 Suggested Additional Reading 236
8 Conclusion: Commonalities and Differences in Life Histories 239 8.1 Levels of Comparison 239 8.2 On Being a Macroorganism or a Microorganism 241 8.3 Natural Selection As the Common Denominator 241 8.4 Microbial Ecology and Macroecology Are
Complementary 245 8.5 Summary 250
Bibliography 251
Index 289
